When confronted with several moving objects, the smooth pursuit system has to integrate information over a region of the visual field to determine the direction of the eye movements. We spatially mapped the influence of different motion vectors with the ultimate goal of finding an ‘oculoceptive field’ of the pursuit system. We asked subjects to pursue a random-dot pattern consisting of 20% correlated signal dots moving rightward or leftward at 10°/s. The pattern was presented inside a circular window with a radius of 20 degrees of visual angle. A perturbation was then added to the pattern, consisting of additional correlated dots moving at an angle offset obliquely upwards or downwards from the pattern direction. The perturbation angle was varied between 5° and 90°, and the perturbation was present throughout the duration of the stimulus in one of 5 regions forming a gaze-contingent circular window with a 10° outer radius and a 2° inner radius. The effect of the perturbation was to deflect the pursuit from the horizontal pattern motion direction into the perturbation direction. The perturbation had the largest effect when the angular difference to the pattern motion direction was small (up to 10°), even though the vertical component of the perturbation was much bigger for larger angular differences. Perturbations with an eccentricity angle larger than 10° tended to be discarded, indicating that this integration is not a simple vector summation process. Rather, motion signals close to the pursuit direction seem to be weighted much heavier than others. Perturbations presented behind the pursuit target had similar effects as those that were ahead of the pursuit target. Our results indicate that the analysis of visual motion during smooth pursuit is focused on the direction of ongoing pursuit. The oculoceptive field for pursuit is centered on the pursuit target.